[en] The present study aimed to characterise the bacterial, fungal and parasite gut community of the invasive bee Megachile sculpturalis sampled from native (Japan) and invaded (USA and France) regions via 16S rRNA and ITS2 amplicon sequencing and PCR detection of bee microparasites. The bacterial and fungal gut microbiota communities in bees from invaded regions were highly similar and differed strongly from those obtained in Japan. Core amplicon sequence variants (ASVs) within each population represented environmental micro-organisms commonly present in bee-associated niches that likely provide beneficial functions to their host. Although the overall bacterial and fungal communities of the invasive M. sculpturalis in France and the co-foraging native bees Anthidium florentinum and Halictus scabiosae, were significantly different, five out of eight core ASVs were shared suggesting common environmental sources and potential transmission. None of the 46 M. sculpturalis bees analysed harboured known bee pathogens, while microparasite infections were common in A. florentinum, and rare in H. scabiosae. A common shift in the gut microbiota of M. sculpturalis in invaded regions as a response to changed environmental conditions, or a founder effect coupled to population re-establishment in the invaded regions may explain the observed microbial community profiles and the absence of parasites. While the role of pathogen pressure in shaping biological invasions is still debated, the absence of natural enemies may contribute to the invasion success of M. sculpturalis.
Disciplines :
Agriculture & agronomy Entomology & pest control
Author, co-author :
Tuerlings, Tina ; Laboratory of Agrozoology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium
Hettiarachchi, Amanda ; Laboratory of Microbiology, Department of Biochemistry and Microbiology, Faculty of Sciences, Ghent University, Ghent, Belgium
Joossens, Marie; Laboratory of Microbiology, Department of Biochemistry and Microbiology, Faculty of Sciences, Ghent University, Ghent, Belgium
Geslin, Benoît; Aix Marseille Univ, Avignon Univ, CNRS, IRD, IMBE, Marseille, France ; Université de Rennes (UNIR), UMR 6553 ECOBIO, CNRS, Rennes, France
Vereecken, Nicolas J; Agroecology Lab, Université Libre de Bruxelles, Brussels, Belgium
MICHEZ, Denis ; Université de Mons - UMONS > Faculté des Sciences > Service de Zoologie
Smagghe, Guy ; Laboratory of Agrozoology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium
Vandamme, Peter ; Laboratory of Microbiology, Department of Biochemistry and Microbiology, Faculty of Sciences, Ghent University, Ghent, Belgium
Language :
English
Title :
Microbiota and pathogens in an invasive bee: Megachile sculpturalis from native and invaded regions.
Fonds Wetenschappelijk Onderzoek F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Funding text :
This work was supported by the FWO and F.R.S.‐FNRS joint program Excellence of Science (EOS) for the project ‘Climate change and its effects on pollination services’ (project number 3094785).
Abarenkov, K., Zirk, A., Piirmann, T., Pöhönen, R., Ivanov, F., Nilsson, R.H. et al. (2021) UNITE general FASTA release for eukaryotes. Version 10.05.2021. UNITE Community. https://doi.plutof.ut.ee/doi/10.15156/BIO/2483911
Alsos, I.G., Ehrich, D., Eidesen, P.B., Solstad, H., Westergaard, K.B., Schönswetter, P. et al. (2015) Long-distance plant dispersal to North Atlantic islands: colonization routes and founder effect. AoB Plants., 7(1), plv036.
Ambika Manirajan, B., Ratering, S., Rusch, V., Schwiertz, A., Geissler-Plaum, R., Cardinale, M. et al. (2016) Bacterial microbiota associated with flower pollen is influenced by pollination type, and shows a high degree of diversity and species-specificity. Environmental Microbiology, 18(12), 5161–5174.
Amiet, F. (2012) Die Blattschneiderbiene Megachile sculpturalis Smith, 1853 (Hymenoptera, Apidae) nun auch in der Schweiz. Entomo Helvetica., 5, 157–159.
An, J.S., Hong, S.H., Somers, E., Lee, J., Kim, B.Y., Woo, D. et al. (2020) Lenzimycins a and B, metabolites with antibacterial properties from Brevibacillus sp. associated with the dung beetle Onthophagus lenzii. Frontiers in Microbiology, 11, 11.
Anjum, S.I., Shah, A.H., Aurongzeb, M., Kori, J., Azim, M.K., Ansari, M.J. et al. (2018) Characterization of gut bacterial flora of Apis mellifera from north-West Pakistan. Journal of Biological Sciences, 25(2), 388–392.
Arbetman, M.P., Meeus, I., Morales, C.L., Aizen, M.A. & Smagghe, G. (2013) Alien parasite hitchhikes to Patagonia on invasive bumblebee. Biological Invasions, 15(3), 489–494.
Arretz, P.v. & Macfarlane, R.P. (1986) The introduction of Bombus ruderatus to Chile for red clover pollination. Bee World, 67(1), 15–22.
Ayyasamy, A., Kempraj, V. & Pagadala Damodaram, K.J. (2021) Endosymbiotic bacteria aid to overcome temperature induced stress in the oriental fruit Fly, Bactrocera dorsalis. Microbial Ecology, 82(3), 783–792.
Behar, A., Yuval, B. & Jurkevitch, E. (2008) Gut bacterial communities in the Mediterranean fruit fly (Ceratitis capitata) and their impact on host longevity. Journal of Insect Physiology, 54(9), 1377–1383.
Bortolotti, L., Luthi, F., Flaminio, S., Bogo, G. & Sgolastra, F. (2018) First record of the Asiatic bee Megachile disjunctiformis in Europe. Bull Insectology., 71(1), 143–149.
Burrows, S., Ritner, C., Christman, M., Spears, L., Smith-Pardo, A., Price, S. et al. (2021) Exotic bee ID.
Ćetković, A. & Plećaš, M. (2017) Dalje širenje alohtone azijske pčele u Evropi: prvi nalaz Megachile sculpturalis na Balkanu. XI Symposium of Entomologists of Serbia.
Chen, M., Vernon, C.R., Graham, N.T., Hejazi, M., Huang, M., Cheng, Y. et al. (2020) Global land use for 2015–2100 at 0.05° resolution under diverse socioeconomic and climate scenarios. Scientific Data., 7(1), 320.
Cini, A., Meriggi, N., Bacci, G., Cappa, F., Vitali, F., Cavalieri, D. et al. (2020) Gut microbial composition in different castes and developmental stages of the invasive hornet Vespa velutina nigrithorax. Science of the Total Environment., 745, 140873.
Cirimotich, C.M., Dong, Y., Clayton, A.M., Sandiford, S.L., Souza-Neto, J.A., Mulenga, M. et al. (1979) Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science, 332(6031), 855–858.
Cohen, H., McFrederick, Q.S. & Philpott, S.M. (2020) Environment shapes the microbiome of the blue orchard bee, Osmia lignaria. Microbial Ecology, 80(4), 897–907.
Colautti, R.I., Ricciardi, A., Grigorovich, I.A. & MacIsaac, H.J. (2004) Is invasion success explained by the enemy release hypothesis? Ecology Letters, 7, 721–733.
da Costa Neto, J. & de Morais, B. (2020) The vectoring of Starmerella species and other yeasts by stingless bees in a Neotropical savanna. Fungal Ecology, 47, 100973.
de Clercq, V., Roelants, S.L.K.W., Castelein, M.G., de Maeseneire, S.L. & Soetaert, W.K. (2021) Elucidation of the natural function of sophorolipids produced by Starmerella bombicola. Journal of Fungi., 7(11), 917.
de Vega, C., Herrera, C.M. & Johnson, S.D. (2009) Yeasts in floral nectar of some South African plants: quantification and associations with pollinator type and sugar concentration. South African Journal of Botany., 75(4), 798–806.
Díaz, S.S., Carisio, L., Manino, A., Biella, P. & Porporato, M. (2021) Nesting, sex ratio and natural enemies of the giant resin bee in relation to native species in Europe. Insects., 12(6), 545.
Dubaić, J.B., Raičević, J., Plećaš, M., Lanner, J., Nikolić, P., Žikić, V. et al. (2021) Further range expansion of the sculptured resin bee (Megachile sculpturalis) in Serbia and Bosnia & Herzegovina. Acta Entomologica Serbica., 26(2), 37–63.
Dunn, A.M. (2009) Parasites and biological invasions. Advances in Parasitology, 68, 161–184.
Ebert, D. (1994) Virulence and local adaptation of a horizontally transmitted parasite. Science, 265(5175), 1084–1086.
Engel, P. & Moran, N.A. (2013) The gut microbiota of insects—diversity in structure and function. FEMS Microbiology Reviews., 37, 699–735.
Fortunato, L., Michele Buian, F., Chiesa, F. & Zandigiacomo, P. (2013) Note biologiche su Anthidium florentinum nell'Italia nord-orientale (Hymenoptera, Megachilidae). Bollettino Soc Naturalisti “Silvia Zenari”, Pordenone, 37, 137–145.
Geng, Y., Wu, W., Li, R., Xu, J., Gu, R., Lu, J. et al. (2021) Founder effects contribute to the population genetic structure of the major dermatophytosis pathogen Trichophyton rubrum on Hainan Island, China. Clinical, Cosmetic and Investigational Dermatology, 14, 1569–1577.
Geslin, B., Gachet, S., Deschamps-Cottin, M., Flacher, F., Ignace, B., Knoploch, C. et al. (2020) Bee hotels host a high abundance of exotic bees in an urban context. Acta Oecologica., 105, 103556.
Gibson, B., Wilson, D.J., Feil, E. & Eyre-Walker, A. (2018) The distribution of bacterial doubling times in the wild. Proceedings of the Royal Society B: Biological Sciences., 285(1880), 20180789.
Gogala, A. & Zadravec, B. (2018) First record of Megachile sculpturalis Smith in Slovenia (Hymenoptera: Megachilidae). Acta Entomologica Slovenica., 26(1), 79–82.
Goulson, D. (2003) Effects of introduced bees on native ecosystems. Annual Review of Ecology, Evolution, and Systematics, 34, 1–26.
Goulson, D. (2010) Impacts of non-native bumblebees in Western Europe and North America. Applied Entomology and Zoology, 45(1), 7–12.
Graystock, P., Rehan, S.M. & McFrederick, Q.S. (2017) Hunting for healthy microbiomes: determining the core microbiomes of Ceratina, Megalopta, and Apis bees and how they associate with microbes in bee collected pollen. Conservation Genetics., 18(3), 701–711.
Gurr, L. (1972) The introduction of bumblebees into North Island, New Zealand. New Zealand Journal of Agricultural Research., 15(3), 635–638.
Halpern, M., Fridman, S., Atamna-Ismaeel, N. & Izhaki, I. (2013) Rosenbergiella nectarea gen. nov., sp. nov., in the family Enterobacteriaceae, isolated from floral nectar. International Journal of Systematic and Evolutionary Microbiology, 63(11), 4259–4265.
Hedrick, P.W., Gutierrez-Espeleta, G.A. & Lee, R.N. (2001) Founder effect in an Island population of bighorn sheep. Molecular Ecology, 10(4), 851–857.
Inglis, G.D., Sigler, L. & Goette, M.S. (1993) Aerobic microorganisms associated with alfalfa leafcutter bees (Megachile rotundata). Microbial Ecology, 26(2), 125–143.
Ivanov, S.P. & Fateryga, A.V. (2019) First record of the invasive giant resin bee Megachile (Callomegachile) sculpturalis smith, 1853 (hymenoptera: Megachilidae) in the Crimea. Far Eastern Entomologist, 395, 7–13.
Iwata, K. (1933) Studies on the nesting habits and parasites of Megachile sculpturalis Smith (Hymenoptera, Megachilidae). Mushi., 6, 4–24.
Johnson, M., Zaretskaya, I., Raytselis, Y., Merezhuk, Y., McGinnis, S. & Madden, T.L. (2008) NCBI BLAST: a better web interface. Nucleic Acids Research, 36(Web Server issue), W5–W9.
Kapheim, K.M., Johnson, M.M. & Jolley, M. (2021) Composition and acquisition of the microbiome in solitary, ground-nesting alkali bees. Scientific Reports, 11(1), 2993.
Kapheim, K.M., Rao, V.D., Yeoman, C.J., Wilson, B.A., White, B.A., Goldenfeld, N. et al. (2015) Caste-specific differences in hindgut microbial communities of honey bees (Apis mellifera). PLoS One, 10(4), e0123911.
Karger, D.N., Conrad, O., Böhner, J., Kawohl, T., Kreft, H., Soria-Auza, R.W. et al. (2017) Climatologies at high resolution for the earth's land surface areas. Scientific Data., 4, 170122.
Keller, A., Grimmer, G. & Steffan-Dewenter, I. (2013) Diverse microbiota identified in whole intact Nest chambers of the red Mason bee Osmia bicornis (Linnaeus 1758). PLoS One, 8(10), e78296.
Keller, A., McFrederick, Q.S., Dharampal, P., Steffan, S., Danforth, B.N. & Leonhardt, S.D. (2021) (More than) Hitchhikers through the network: the shared microbiome of bees and flowers. Current Opinion in Insect Science, 44, 8–15.
Khalil, A.B., Sivakumar, N., Arslan, M., Saleem, H. & Qarawi, S. (2018) Insights into Brevibacillus borstelensis AK1 through whole genome sequencing: a thermophilic bacterium isolated from a hot spring in Saudi Arabia. BioMed Research International, 2018, 1–9.
Kishimoto, N., Kosako, Y., Wakao, N., Tano, T. & Hiraishi, A. (1995) Transfer of Acidiphilium facilis and Acidiphilium aminolytica to the genus Acidocella gen. nov., and emendation of the genus Acidiphilium. Systematic and Applied Microbiology, 18(1), 85–91.
König, H. (2006) Bacillus species in the intestine of termites and other soil invertebrates. Journal of Applied Microbiology., 101, 620–627.
Kovács, T. (2015) Megachile sculpturalis Smith, 1853 in Hungary (Hymenoptera, Megachilidae). Folio Historico-Naturalia Musei Matraensis., 39, 73–76.
Kurtzman, C.p., Fell, J.W. & Boekhout, T. (2011) Definition, classification and nomenclature of the yeasts. In: The yeasts: A taxonomic study, 5th ed., Vol. 1–3. Burlington: Elsevier Science.
Lachance, M.A., Starmer, W.T., Rosa, C.A., Bowles, J.M., Barker, J.S.F. & Janzen, D.H. (2001) Biogeography of the yeasts of ephemeral flowers and their insects. FEMS Yeast Research., 1, 1–8.
Lanner, J., Dubos, N., Geslin, B., Leroy, B., Hernández-Castellano, C., Dubaić, J.B. et al. (2022) On the road: anthropogenic factors drive the invasion risk of a wild solitary bee species. Science of the Total Environment., 827, 154246.
Lanner, J., Gstöttenmayer, F., Curto, M., Geslin, B., Huchler, K., Orr, M.C. et al. (2021) Evidence for multiple introductions of an invasive wild bee species currently under rapid range expansion in Europe. BMC Evolutionary Biology., 21(1), 17.
Lanner, J., Huchler, K., Pachinger, B., Sedivy, C. & Meimberg, H. (2020) Dispersal patterns of an introduced wild bee, Megachile sculpturalis Smith, 1853 (Hymenoptera: Megachilidae) in European alpine countries. PLoS One, 15(7), e0236042.
Laport, R.G. & Minckley, R.L. (2012) Occupation of active Xylocopa virginica nests by the recently invasive Megachile sculpturalis in upstate New York. Journal of the Kansas Entomological Society, 85(4), 384–386.
Laviad-Shitrit, S., Izhaki, I., Whitman, W.B., Shapiro, N., Woyke, T., Kyrpides, N.C. et al. (2020) Draft genome of Rosenbergiella nectarea strain 8N4T provides insights into the potential role of this species in its plant host. PeerJ, 2020(4), e8822.
Le Féon, V., Aubert, M., Genoud, D., Andrieu-Ponel, V., Westrich, P. & Geslin, B. (2018) Range expansion of the Asian native giant resin bee Megachile sculpturalis (Hymenoptera, Apoidea, Megachilidae) in France. Ecology and Evolution, 8(3), 1534–1542.
Le Féon, V., Genoud, D. & Geslin, B. (2021) Actualisation des connaissances sur l'abeille Megachile sculpturalis SMITH, 1853 en France et en Europe (Hymenoptera: Megachilidae). Journal of Hymenopterology, 9, 25–36.
Lemos Junior, W.J.F., Binati, R.L., Felis, G.E., Slaghenaufi, D., Ugliano, M. & Torriani, S. (2020) Volatile organic compounds from Starmerella bacillaris to control gray mold on apples and modulate cider aroma profile. Food Microbiology, 89, 103446.
Lenaerts, M., Álvarez-Pérez, S., de Vega, C., van Assche, A., Johnson, S.D., Willems, K.A. et al. (2014) Rosenbergiella australoborealis sp. nov., Rosenbergiella collisarenosi sp. nov. and Rosenbergiella epipactidis sp. nov., three novel bacterial species isolated from floral nectar. Systematic and Applied Microbiology, 37(6), 402–411.
Lombogia, C.A., Tulung, M., Posangi, J. & Tallei, T.E. (2020) Bacterial composition, community structure, and diversity in Apis nigrocincta gut. International Journal of Microbiology, 2020, 1–8.
Love, M.I., Huber, W. & Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15(12), 550.
Maebe, K., Vereecken, N.J., Piot, N., Reverté, S., Cejas, D., Michez, D. et al. (2021) The Holobiont as a key to the adaptation and conservation of wild bees in the Anthropocene. Frontiers in Ecology and Evolution., 9, 781470.
Maharramov, J., Meeus, I., Maebe, K., Arbetman, M., Morales, C., Graystock, P. et al. (2013) Genetic variability of the neogregarine Apicystis bombi, an etiological agent of an emergent bumblebee disease. PLoS One, 8(12), e81475.
Mangum, W.A. & Brooks, R.W. (1997) First records of Megachile (Callomegachile) sculpturalis Smith (Hymenoptera: Megachilidae) in the continental United States. Journal of the Kansas Entomological Society, 70(2), 140–142.
Mangum, W.A. & Sumner, S. (2003) A survey of the North American range of Megachile (Callomegachile) sculpturalis, an adventive species in North America. Journal of the Kansas Entomological Society, 76(4), 658–662.
Marche, M.G., Mura, M.E. & Ruiu, L. (2016) Brevibacillus laterosporus inside the insect body: beneficial resident or pathogenic outsider? Journal of Invertebrate Pathology, 137, 58–61.
Martin, M. (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. Journal, 17(1), 10.
Matteson, K.C., Ascher, J.S. & Langellotto, G.A. (2008) Bee richness and abundance in New York City urban gardens. Annals of the Entomological Society of America, 101(1), 140–150.
McFrederick, Q.S., Vuong, H.Q. & Rothman, J.A. (2018) Lactobacillus micheneri sp. nov., Lactobacillus timberlakei sp. nov. and Lactobacillus quenuiae sp. nov., lactic acid bacteria isolated from wild bees and flowers. International Journal of Systematic and Evolutionary Microbiology, 68(6), 1879–1884.
McLaren, M.R. & Callahan, B.J. (2021) Silva 138.1 prokaryotic SSU taxonomic training data formatted for DADA2. Vol. 1, Zenodo.
McMurdie, P.J. & Holmes, S. (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8(4), e61217.
Meeus, I., Brown, M.J.F., de Graaf, D.C. & Smagghe, G. (2011) Effects of invasive parasites on bumble bee declines. Conservation Biology., 25, 662–671.
Meurisse, N., Rassati, D., Hurley, B.P., Brockerhoff, E.G. & Haack, R.A. (2019) Common pathways by which non-native forest insects move internationally and domestically. Journal of Pest Science., 92, 13–27.
Michez, D., Rasmont, P., Terzo, M. & Vereecken, N.J. (2019) Bees of Europe. Paris, France: NAP Editions.
Miller, D.L., Smith, E.A. & Newton, I.L.G. (2021) A bacterial symbiont protects honey bees from fungal disease. MBio, 12(3), e0050321.
Morimoto, T., Kojima, Y., Yoshiyama, M., Kimura, K., Yang, B., Peng, G. et al. (2013) Molecular detection of protozoan parasites infecting Apis mellifera colonies in Japan. Environmental Microbiology Reports, 5(1), 74–77.
Muhammad, A., Fang, Y., Hou, Y. & Shi, Z. (2017) The gut entomotype of red palm weevil Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae) and their effect on host nutrition metabolism. Frontiers in Microbiology, 8, 2291.
Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., Mcglinn, D. et al. (2020) Package ‘vegan’ title community ecology package version 2.5-7.
Ortiz-Sánchez, F.J., Navarro, J.F. & Taeger, U. (2018) Megachile (Callomegachile) sculpturalis Smith, 1853, nueva especie para la fauna Ibérica (Hymenoptera, Megachilidae). Boletín de la Sociedad Entomológica Aragonesa, 63, 259–261.
Paiero, S.M. & Buck, M. (2003) The Giant resin bee, Megachile sculpturalis Smith, and other newly introduced and newly recorded native Megachilidae and Andrenidae (Apoidea) from Ontario. Journal of the Entomological Society of Ontario, 134, 143.
Paludo, C.R., Menezes, C., Silva-Junior, E.A., Vollet-Neto, A., Andrade-Dominguez, A., Pishchany, G. et al. (2018) Stingless bee larvae require fungal steroid to pupate. Scientific Reports, 8(1), 1122.
Parker, J.D., Torchin, M.E., Hufbauer, R.A., Lemoine, N.P., Alba, C., Blumenthal, D.M. et al. (2013) Do invasive species perform better in their new ranges? Ecology, 94(5), 985–994.
Parys, K.A., Tripodi, A.D. & Sampson, B.J. (2015) The Giant resin bee, Megachile sculpturalis Smith: new distributional records for the mid- and Gulfsouth USA. Biodiversity Data Journal, 3(1), e6733.
Passerini, D., Coddeville, M., le Bourgeois, P., Loubière, P., Ritzenthaler, P., Fontagné-Faucher, C. et al. (2013) The carbohydrate metabolism signature of Lactococcus lactis strain A12 reveals its sourdough ecosystem origin. Applied and Environmental Microbiology, 79(19), 5844–5852.
Pimentel, M.R.C., Antonini, Y., Martins, R.P., Lachance, M.A. & Rosa, C.A. (2005) Candida riodocensis and Candida cellae, two new yeast species from the Starmerella clade associated with solitary bees in the Atlantic rain forest of Brazil. FEMS Yeast Research, 5(9), 875–879.
Pitts-Singer, T.L. & Cane, J.H. (2011) The alfalfa leafcutting bee, Megachile rotundata: the world's most intensively managed solitary bee. Annual Review of Entomology, 56, 221–237.
Pozo, M.I., Herrera, C.M., Lachance, M.A., Verstrepen, K., Lievens, B. & Jacquemyn, H. (2016) Species coexistence in simple microbial communities: unravelling the phenotypic landscape of co-occurring Metschnikowia species in floral nectar. Environmental Microbiology, 18(6), 1850–1862.
Quaranta, M., Sommaruga, A., Balzarini, P. & Felicioli, A. (2014) A new species for the bee fauna of Italy: Megachile sculpturalis continues its colonization of Europe. Bull Insectology., 67(2), 287–293.
Rering, C.C., Beck, J.J., Hall, G.W., McCartney, M.M. & Vannette, R.L. (2018) Nectar-inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator. New Phytologist., 220(3), 750–759.
Rosa, C.A., Jindamorakot, S., Limtong, S., Nakase, T., Lachance, M.A., Fidalgo-Jiménez, A. et al. (2009) Synonymy of the yeast genera Moniliella and Trichosporonoides and proposal of Moniliella fonsecae sp. nov. and five new species combinations. International Journal of Systematic and Evolutionary Microbiology, 59(2), 425–429.
Rosa, C.A., Pagnocca, F.C., Lachance, M.A., Ruivo, C.C.C., Medeiros, A.O., Pimentel, M.R.C. et al. (2007) Candida flosculorum sp. nov. and Candida floris sp. nov., two yeast species associated with tropical flowers. International Journal of Systematic and Evolutionary Microbiology, 57(12), 2970–2974.
Roulston, T. & Malfi, R. (2012) Aggressive eviction of the eastern carpenter bee (Xylocopa virginica (Linnaeus)) from its nest by the giant resin bee (Megachile sculpturalis Smith). Journal of the Kansas Entomological Society, 85(4), 387–388.
Russo, L. (2016) Positive and negative impacts of non-native bee species around the world. Insects., 7(4), 69.
Santos, A.R.O., Leon, M.P., Barros, K.O., Freitas, L.F.D., Hughes, A.F.S., Morais, P.B. et al. (2018) Starmerella camargoi f.a., sp. nov., Starmerella ilheusensis f.a., sp. nov., Starmerella litoralis f.a., sp. nov., Starmerella opuntiae f.a., sp. nov., Starmerella roubikii f.a., sp. nov. and Starmerella vitae f.a., sp. nov., isolated from flowers and bees, and transfer of related Candida species to the genus Starmerella as new combinations. International Journal of Systematic and Evolutionary Microbiology, 68(4), 1333–1343.
Schoonvaere, K., Brunain, M., Baeke, F., de Bruyne, M., de Rycke, R. & de Graaf, D.C. (2020) Comparison between Apicystis cryptica sp. n. and Apicystis bombi (Arthrogregarida, Apicomplexa): gregarine parasites that cause fat body hypertrophism in bees. European Journal of Protistology, 73, 125688.
Seebens, H., Blackburn, T.M., Dyer, E.E., Genovesi, P., Hulme, P.E., Jeschke, J.M. et al. (2017) No saturation in the accumulation of alien species worldwide. Nature Communications, 8, 14435.
Singh, P. & Kumar, S. (2018) Microbial enzyme in food biotechnology. In: Enzymes in food biotechnology: production, applications, and future prospects. Cambridge, Massachusetts: Academic Press.
Sipiczki, M. (2020) Metschnikowia pulcherrima and related pulcherrimin-producing yeasts: fuzzy species boundaries and complex antimicrobial antagonism. Microorganisms, 8, 1029.
Snauwaert, I., Roels, S.P., van Nieuwerburgh, F., van Landschoot, A., de Vuyst, L. & Vandamme, P. (2016) Microbial diversity and metabolite composition of Belgian red-brown acidic ales. International Journal of Food Microbiology, 221, 1–11.
Stahly, D.P., Andrews, R.E. & Yousten, A.A. (2006) The genus Bacillus—insect pathogens. In: The prokaryotes. New York: Springer New York.
Thanh, V.N. & Hien, D.D. (2019) Moniliella floricola sp. nov., a species of black yeast isolated from flowers. International Journal of Systematic and Evolutionary Microbiology, 69(1), 87–92.
Torchin, M.E., Lafferty, K.D., Dobson, A.P., McKenzie, V.J. & Kuris, A.M. (2003) Introduced species and their missing parasites. Nature, 421(6923), 628–630.
Torchio, P.F., Asensio, E. & Thorp, R.W. (1987) Introduction of the European bee, Osmia cornuta, into California almond orchards (Hymenoptera: Megachilidae). Environmental Entomology, 16(3), 664–667.
Vereecken, N.J. & Barbier, É. (2009) Premières données sur la présence de l'abeille asiatique Megachile (Callomegachile) sculpturalis Smith (Hymenoptera, Megachilidae) en Europe. Osmia., 3, 3–6.
Voulgari-Kokota, A., Ankenbrand, M.J., Grimmer, G., Steffan-Dewenter, I. & Keller, A. (2019) Linking pollen foraging of megachilid bees to their nest bacterial microbiota. Ecology and Evolution, 9(18), 10788–10800.
Voulgari-Kokota, A., Grimmer, G., Steffan-Dewenter, I. & Keller, A. (2018) Bacterial community structure and succession in nests of two megachilid bee genera. FEMS Microbiology Ecology, 95(1), fiy218.
Wels, M., Siezen, R., van Hijum, S., Kelly, W.J. & Bachmann, H. (2019) Comparative genome analysis of Lactococcus lactis indicates niche adaptation and resolves genotype/phenotype disparity. Frontiers in Microbiology, 10, 4.
Westrich, P. (2015) Megachile sculpturalis Smith 1853 (Hymenoptera, Apidae), a new species for the bee fauna of Germany, now north of the Alps. Eucera., 9, 3–10.
Wirtz, P., Kopka, S. & Schmoll, G. (1992) Phenology of two territorial solitary bees, Anthidium manicatum and A. florentinum (Hymenoptera: Megachilidae). Journal of Zoology, 228(4), 641–651.
Yang, M., Deng, G.C., Gong, Y.B. & Huang, S.Q. (2019) Nectar yeasts enhance the interaction between Clematis akebioides and its bumblebee pollinator. Plant Biology, 21(4), 732–737.
Yang, X. & Yousef, A.E. (2018) Antimicrobial peptides produced by Brevibacillus spp.: structure, classification and bioactivity: a mini review. World Journal of Microbiology and Biotechnology, 34, 57.
Yun, J.H., Jung, M.J., Kim, P.S. & Bae, J.W. (2018) Social status shapes the bacterial and fungal gut communities of the honey bee. Scientific Reports, 8(1), 2019.
